Color profile: Disabled Composite Default screen 77 Movement, migration, and smolting of Atlantic salmon (Salmo salar) Stephen D. McCormick, Lars P. Hansen, Thomas P. Quinn, and Richard L. Saunders Abstract: A variety of movements characterize the behavioral plasticity of Atlantic salmon (Salmo salar) in fresh water, including movements of fry from redds, establishment of feeding territories, spawning movements of sexually mature male parr, movement to and from winter habitat, and smolt migration in spring. Smolting is an adaptive specialization for downstream migration, seawater entry, and marine residence. While still in fresh water, smolts become silvery and streamlined, lose their positive rheotaxis and territoriality, and begin schooling. Physiological changes include increased salinity tolerance, olfactory sensitivity, metabolic rate, scope for growth, and altered hemoglobin and visual pigments. Through their impact on the neuroendocrine system, photoperiod and temperature regulate physiological changes, whereas temperature and water flow may initiate migration. Smolt survival is affected by a limited period of readiness (a physiological “smolt window”) and the timing of seawater entry with environmental conditions such as temperature, food, and predators (an ecological “smolt window”). Smolt development is adversely affected by acidity, pollutants, and improper rearing conditions, and is often more sensitive than other life stages. Unfortunately, the migration corridor of smolts (mainstems of rivers and estuaries) are the most heavily impacted by pollution, dams, and other anthropogenic activities that may be directly lethal or increase mortality by delaying or inhibiting smolt migration. Résumé: Une grande variété de déplacements caractérise la plasticité comportementale du saumon de l’Atlantique en eau douce, notamment le départ des alevins qui quittent le nid, l’établissement de territoires d’alimentation, les déplacements génésiques des tacons mâles sexuellement matures, les allers-retours vers les zones d’hivernage, et la dévalaison des smolts au printemps. La smoltification est une spécialisation adaptative enn vue de la dévalaison, de l’entrée dans l’eau salée, et du séjour océanique. Alors qu’ils sont encore en eau douce, les smolts prennent leur livrée argentée et leur forme devient plus hydrodynamique, ils perdent leur rhéotaxie positive et leur territorialité, et commencent à se rassembler en bancs. Ils subissent des changements d’ordre physiologique : tolérance accrue à la salinité, sensibilité olfactive, métabolisme, potentiel de croissance et modification de l’hémoglobine et des pigments visuels. Par leur impact sur le système neuroendocrinien, la photopériode et la température régulent les changements physiologiques, tandis que la température et le débit peuvent déclencher la migration. La survie des smolts est affectée par l’existence d’une période limitée de condition optimale (une « fenêtre physiologique ») et par la synchronisation de l’entrée en eau salée avec des conditions environnementales comme la température, la nourriture, et la présence de prédateurs (une « fenêtre écologique »). Le développement des smolts est négativement affecté par l’acidité, les polluants, et les mauvaises conditions de grossissement, et ce stade est souvent plus vulnérable que les autres. Malheureusement, le corridor de migration des smolts (cours principal des cours d’eau et estuaires) passe par les eaux les plus fortement touchées par la pollution, les barrages, et d’autres activités humaines qui peuvent avoir un effet létal direct ou accroître la mortalité en retardant ou en empêchant la migration des jeunes saumons. [Traduit par la Rédaction] McCormick et al. 92 Received November 7, 1997. Accepted September 30, 1998. J14300 Migration is the hallmark of salmon life history. When ju- S.D. McCormick.1 Conte Anadromous Fish Research Center, venile Atlantic salmon (Salmo salar) reach a certain size- Biological Resources Division, USGS, P.O. Box 796, Turners related developmental stage in fresh water, they leave their Falls, MA 01376, U.S.A. rearing tributaries in spring and begin a journey that will L.P. Hansen. Norwegian Institute for Nature Research, Oslo, take them downriver, through estuaries, and hundreds or Norway. thousands of kilometres to ocean feeding areas. Prior to and T.P. Quinn. School of Fisheries, University of Washington, during this downstream movement, they display many com- Seattle, WA 09195, U.S.A. R.L. Saunders. St. Andrews Biological Station, Department plex physiological, behavioral, and morphological adapta- of Fisheries and Oceans, St. Andrews, NB E0G 2X0, tions for seaward migration and life at sea. Along with these Canada. complex changes, smolts face other challenges: new food sources, diseases, parasites, and predators, which make the smolt stage a critical one in which mortality can be high and 1Author to whom all correspondence should be addressed. variable. Growth opportunities for salmonids are generally e-mail: [email protected] better at sea than in fresh water, but natural mortality may be Can. J. Fish. Aquat. Sci. 55(Suppl. 1): 77–92 (1998) © 1998 NRC Canada I:\Salmon Sup\D98-011.vp Wednesday, February 10, 1999 11:46:51 AM Color profile: Disabled Composite Default screen 78 Can. J. Fish. Aquat. Sci. Vol. 55(Suppl. 1), 1998 higher in the marine environment. The “decision” as to Fig. 1. Movement patterns of Atlantic salmon. Filled area whether the population or individual gains greater advantage represents the range of estimated distances travelled for a given from migration or residence depends on the balance of these life history stage. A representative 4-year life cycle (2-year-old two factors (see Jonsson and Jonsson 1993; Thorpe 1994). smolt) is shown on the x-axis (W = winter, S = spring and The much greater fecundity of anadromous females and re- summer, F = fall). Relative values for distance travelled are duced mortality of eggs and fry in fresh water are the appar- approximate and taken from literature discussed in section on ent rewards for undertaking the risks of anadromy (Gross “Fry and parr movement.” Smolt migration distance includes 1987). both river and initial ocean migration. In addition to the smolt migration, Atlantic salmon make other movements in fresh water that are important to their survival (Fig. 1 and next section), including movements to winter habitat and spawning movements of mature parr. Be- cause smolting, winter survival, and sexual maturation re- quire high levels of stored energy, feeding and growth are of prime importance during freshwater residence. Movements, then, are mainly associated with attaining the maximum amount of food or a suitable habitat while avoiding preda- tion or other sources of mortality. The downstream movement of smolts is a “true” migra- tion, being highly directed, temporally synchronous, and oc- curring in virtually all individuals of the appropriate developmental stage. It is less clear whether the movements made by Atlantic salmon before smolting are migrations and no single definition of this term is accepted by all or even most biologists. Dingle (1996) defined migratory behavior the smolt stage and discusses possible motivations for these as “persistent and straightened-out movement effected by the behaviors. We also describe the smolting process in terms of animal’s own locomotory exertions or by its active embarka- physiology, morphology, and behavior and discuss the pos- tion on a vehicle. It depends on some temporary inhibition sible role of olfactory imprinting in relation to these factors. of station-keeping responses, but promotes their eventual Finally, some factors affecting the mortality of smolts during disinhibition and recurrence.” He also considered that migra- downstream migration and the transition from fresh to salt tion is persistent, straightened-out (directed), undistracted by water are reviewed and fruitful areas of future research are resources that would ordinarily halt it, has distinct departing presented. and arriving behavior, and requires a special allocation of energy. Under these terms, salmon movements in fresh water would not be considered migrations unless they were di- rected (e.g., upstream or downstream) and could not be We have divided the movements of juvenile Atlantic stopped by encountering a particular resource (e.g., habitat salmon prior to the smolt transformation into five phases: or food). We do not know whether all Atlantic salmon (1) movement of fry from the vicinity of their redds; (2) es- movements fulfill this definition, but in many cases they tablishment and occupation of feeding territories; (3) spawn- clearly do not. While it is beyond the scope of the present ing movements of sexually mature male parr; (4) shifting undertaking to classify salmon movements, we will conser- from summer feeding territories to winter habitat; and vatively interpret most (but not all) nonsmolt movements in (5) descent from nursery streams to lower reaches of some fresh water as meeting the more general criteria of “move- rivers in late autumn as a forerunner or component of smolt ment” rather than the more restrictive “migration.” Although migration. some of these considerations are semantic, they facilitate our understanding of the external stimuli and internal motivation Movement of fry from redds that underlie the initiation and cessation of juvenile salmon Spawning areas are typically gravel beds with moderate movements. current velocity and depth (Fleming 1996). When